Skip to main content
Log in

Molecular Adaptation in the Ice Worm, Mesenchytraeus solifugus: Divergence of Energetic-Associated Genes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The ice worm, Mesenchytraeus solifugus, is the largest glacially obligate metazoan and among only a few metazoan species that complete their life cycle at 0°C. We conducted a large-scale sequencing analysis of cDNAs isolated from ice worm anterior segments. Sequence comparisons among an available group of ice worm, arthropod, chordate, and nematode homologues suggest that ice worms encode proteins that are less bulky, are less polar, and contain fewer charged residues. Also, subunits of the catalytic F1 ATP synthase complex appear to have diverged more rapidly than other ice worm genes examined, suggesting a role in cold-temperature adaptation. Modeling of F1 ATP synthase β and γ subunits identified nonconservative, ice worm-specific amino acid substitutions at subunit contact sites and at sites proximal to the catalytic site.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • JP Abrahams AGW Leslie R Lutter JE Walker (1994) ArticleTitleStructure at 2.8Å resolution of F1-ATPase from bovine heart mitochondria Nature 370 621–628 Occurrence Handle10.1038/370621a0 Occurrence Handle1:CAS:528:DyaK2cXmt1Cqsbo%3D Occurrence Handle8065448

    Article  CAS  PubMed  Google Scholar 

  • RM Adkins RL Honeycutt TR Disotell (1996) ArticleTitleEvolution of eurtherian cytochrome c oxidase subunit II: Heterogeneous rates of protein evolution and altered interaction with cytochrome c Mol Biol Evol 13 1394–1404

    Google Scholar 

  • SF Altschul W Gish W Miller EW Myers DJ Lipman (1990) ArticleTitleBasic Local Alignment Search Tool J Mol Biol 3 403–410

    Google Scholar 

  • M Alvarez JP Zeelen V Mainfroid F Rentier-Delrue JA Martial L Wyns RK Wierenga D Maes (1998) ArticleTitleTriose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties J Biol Chem 273 2199–2106

    Google Scholar 

  • TD Andrews S Easteal (2000) ArticleTitleEvolutionary rate acceleration of cytochrome c oxidase subunit 1 in simian primates J Mol Evol 50 562–568

    Google Scholar 

  • TD Andrews LS Jermiin S Easteal (1998) ArticleTitleAccelerated evolution of cytochrome b in simian primates: Adaptive evolution in concert with other mitochondrial proteins? J Mol Evol 47 249–257

    Google Scholar 

  • DE Atkinson (1977) Cellular Energy Metabolism and Its Regulation Academic Press New York

    Google Scholar 

  • FM Ausubel R Brent RE Kingston DD Moore (1999) Current Protocols in Molecular Biology John Wiley & Sons New York

    Google Scholar 

  • FJ Ayala (1997) ArticleTitleVagaries of the molecular clock Proc Natl Acad Sci USA 94 7776–7783

    Google Scholar 

  • FJ Ayala A Rzhetsky (1998) ArticleTitleOrigin of the metazoan phyla: Molecular clocks confirm paleontological estimates Proc Natl Acad Sci USA 95 606–611

    Google Scholar 

  • J Belehradek (1935) Temperature and Living Matter Gebruder Borntraeger, Berlin

    Google Scholar 

  • HM Berman J Westbrook Z Feng G Gilliland TN Bhat H Weissig IN Shindyalov PE Bourne (2000) ArticleTitleThe Protein Data Bank Nucleic Acid Res 28 235–242

    Google Scholar 

  • R Chenna H Sugawara T Koike R Lopez TJ Gibson DG Higgins JD Thompson (2003) ArticleTitleMultiple sequence alignment with the Clustal series of programs Nucleic Acids Res 31 3497–3500 Occurrence Handle10.1093/nar/gkg500 Occurrence Handle1:CAS:528:DC%2BD3sXltVWjsrg%3D Occurrence Handle12824352

    Article  CAS  PubMed  Google Scholar 

  • P Chomczynski N Sacchi (1987) ArticleTitleSingle-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal Biochem 162 156–159 Occurrence Handle10.1006/abio.1987.9999 Occurrence Handle1:CAS:528:DyaL2sXitFSns7Y%3D Occurrence Handle2440339

    Article  CAS  PubMed  Google Scholar 

  • S D’Amico P Claverie T Collins D Georlette E Gratia A Hoyoux M Meuwis G Feller C Gerday (2002) ArticleTitleMolecular basis of cold adaptation Philos Trans R Soc Lond B 357 917–925

    Google Scholar 

  • G Feller Z Zekhnini J Lamotte-Brausseur C Gerday (1997) ArticleTitleEnzymes from cold-adapted micro-organisms The class C′′-lactamase from the antarctic psychrophile Psychrobacter immobilis A5 Eur J Biochem 244 186–191

    Google Scholar 

  • KG Field GJ Olsen DJ Lane SJ Giovannoni MT Ghiselin EC Raff NR Race RA Raff (1988) ArticleTitleMolecular phytogeny of the animal kingdom Science 239 748–753 Occurrence Handle1:CAS:528:DyaL1cXhsVKltb8%3D Occurrence Handle3277277

    CAS  PubMed  Google Scholar 

  • E Gasteiger A Gattiker C Hoogland I Ivanyi RD Appel A Bairoch (2003) ArticleTitleExPASy: The proteomics server for in-depth protein knowledge and analysis Nucleic Acids Res 31 3784–3788 Occurrence Handle10.1093/nar/gkg563 Occurrence Handle1:CAS:528:DC%2BD3sXltVWjtLc%3D Occurrence Handle12824418

    Article  CAS  PubMed  Google Scholar 

  • G Gianese P Argos S Pascarella (2001) ArticleTitleStructural adaptation of enzymes to low temperatures Protein Eng 14 141–148

    Google Scholar 

  • G Giribet (2002) ArticleTitleCurrent advances in the phylogenetic reconstruction of metazoan evolution. A new paradigm for the Cambrian explosion? Mol Phylog Evol 24 345–357

    Google Scholar 

  • Goodman D (1971) Ecological investigations of ice worms on Casement Glacier, Southeast Alaska. Rep. No. 39, Institute of Polar Studies. Ohio State University Research Foundation, Columbus pp 1–59

  • SJ Gould N Eldredge (1993) ArticleTitlePunctuated equilibrium comes of age Nature 366 223–227

    Google Scholar 

  • E Gudmundsdottir R Spilliaert Q Yang CS Craik JB Bjarnason A Gudmundsdottir (1996) ArticleTitleIsolation and characterization of two cDNAs from Atlantic cod encoding two distinct psychrophilic elastes Comp Biochem Physiol B 113 795–801

    Google Scholar 

  • PL Haney JH Badger GL Buldak CI Reich CR Woese GJ Olsen (1999) ArticleTitleThermal adaptation analyzed by comparison of protein sequences from mesophilic and extemely thermophilic Methanococcus species Proc Natl Acad Sci USA 96 3578–3583

    Google Scholar 

  • W Kaplan TG Littlejohn (2001) ArticleTitleSwiss-PDB Viewer (Deep View): Biomolecular graphics Brief Bioinform 2 195–197

    Google Scholar 

  • JA Leyva (2003) ArticleTitleUnderstanding ATP synthesis: Structure and mechanism of the F1-ATPase Mol Membr Biol 20 27–33

    Google Scholar 

  • CJ Marshall (1997) ArticleTitleCold-adapted enzymes Trends Biotech 15 359–364

    Google Scholar 

  • RI Menz JE Walker AGW Leslie (1994) ArticleTitleStructure of bovine mitochondrial F1-ATPase with nucleotide bound to all three catalytic sites: Implications for the mechanism of rotary catalysis Cell 106 331–341

    Google Scholar 

  • S Moller MD Croning R Apweiler (2001) ArticleTitleEvaluation of methods for the prediction of membrane spanning regions Bioinformatics 17 646–653

    Google Scholar 

  • SC Morris (1997) ArticleTitleMolecular clocks: Defusing the Cambrian “explosion”? Curr Biol 7 R71–R74

    Google Scholar 

  • MJ Napolitano RO Nagele DH Shain (2004) ArticleTitleIce worms elevate adenylate levels at low physiological temperature Comp Biochem Physiol A 137 227–235

    Google Scholar 

  • DG Nicholls SJ Ferguson (2002) Bioenergetics 3 Academic Press London 195–217

    Google Scholar 

  • Y Nishio Y Nakamura Y Kawarabayasi Y Usuda E Kimura S Sugimoto K Matsui A Yamagishi K Kikuchi H Ikeo T Gojobori (2003) ArticleTitleComparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficients Genome Res 13 1572–1579 Occurrence Handle10.1101/gr.1285603 Occurrence Handle1:CAS:528:DC%2BD3sXls1Krurw%3D Occurrence Handle12840036

    Article  CAS  PubMed  Google Scholar 

  • RA Sayle EJ Milner-White (1995) ArticleTitleRasMol: Biomolecular graphics for all Trends Biochem Sci 20 374–376 Occurrence Handle10.1016/S0968-0004(00)89080-5 Occurrence Handle1:CAS:528:DyaK2MXotF2rsLg%3D Occurrence Handle7482707

    Article  CAS  PubMed  Google Scholar 

  • AO Smalas HS Leiros V Os NP Willassen (2000) ArticleTitleCold adapted enzymes Biotech Annu Rev 6 1–57

    Google Scholar 

  • DH Shain MR Carter KP Murray KA Maleski NR Smith TR McBride LA Michalewicz WM Saidel (2000) ArticleTitleMorphologic characterization of the ice worm (Mesenchytraeus solifugus) J Morphol 246 192–197

    Google Scholar 

  • DH Shain TA Mason AH Farrell LA Michalewicz (2001) ArticleTitleDistribution and behavior of ice worms (Mesenchytraeus solifusus) in south-central Alaska Can J Zool 79 1813–1821

    Google Scholar 

  • NGC Smith A Eyre-Walker (2001) ArticleTitleA test of amino acid reversibility J Mol Evol 52 467–469

    Google Scholar 

  • V Sobolev A Sorokine J Prilusky EE Abola M Edelman (1999) ArticleTitleAutomated analysis of interatomic contacts in proteins. Ligand–protein contacts Bioinformatics 15 327–332

    Google Scholar 

  • F Tekaia E Yeramian B Dujon (2002) ArticleTitleAmino acid composition of genomes, lifestyles of organisms, and evolutionary trends: A global picture with correspondence analysis Gene 297 51–60

    Google Scholar 

  • MJ Tynen (1970) ArticleTitleWorms on ice Nature 225 557

    Google Scholar 

Download references

Acknowledgments

We thank Jefferson Nghiem and Dr. Patrick McIlroy for assistance with protein modeling. This work was supported in part by National Geographic Society Grant 6734-00 to D.H.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel H. Shain.

Additional information

Reviewing Editor: Dr. Graziano Pesole

(Angela H. Farrell and Kristi A. Hohenstein) These authors contributed equally.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Farrell, A.H., Hohenstein, K.A. & Shain, D.H. Molecular Adaptation in the Ice Worm, Mesenchytraeus solifugus: Divergence of Energetic-Associated Genes. J Mol Evol 59, 666–673 (2004). https://doi.org/10.1007/s00239-004-2658-z

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-2658-z

Keywords

Navigation